Spread of Influenza Virus A (H5N1) Clade 2.3.2.1 to Bulgaria in Common Buzzards

Abstract

On March 15, 2010, a highly pathogenic avian influenza virus was isolated from the carcass of a common buzzard (Buteo buteo) in Bulgaria. Phylogenetic analyses of the virus showed a close genetic relationship with influenza virus A (H5N1) clade 2.3.2.1 viruses isolated from wild birds in the Tyva Republic and Mongolia during 2009–2010. Designated A/common buzzard/Bulgaria/38WB/2010, this strain was highly pathogenic in chickens but had low pathogenicity in mice and ferrets and no molecular markers of increased pathogenicity in mammals. The establishment of clade 2.3.2.1 highly pathogenic avian influenza viruses of the H5N1 subtype in wild birds in Europe would increase the likelihood of health threats to humans and poultry in the region.

Excerpt:

Migration of common buzzards in different parts of Europe appears to depend on the local climate; buzzards from northern Europe fly to the western Black Sea area during the winter season, whereas buzzards from Bulgaria fly south. Tracking bands belonging to common buzzards from Finland, Romania, and Israel have been found in Bulgaria (39). The buzzard infected with HPAIV (H5N1) in Bulgaria was not banded; however, even if it had been a migrant, the habitat nearest to St. Konstantin and Helena Black Sea Resort that provides different food sources is Batova, with an area of 38,132.8 ha (35). The migration of the common buzzards suggests that these birds are capable of spreading pathogens over long distances.

Our results show that chickens are highly susceptible to influenza virus A/common buzzard/Bulgaria/38WB/2010 (H5N1) and that the virus is highly pathogenic in them. Mammals appear not to be susceptible. Although buzzards can serve as intermediate hosts of HPAIV (H5N1) between migratory birds and poultry, the lack of gross pathologic findings in the buzzard carcass we examined indicates that the bird died shortly after infection. Thus, in this case, the buzzard could not have served as a reservoir of infection to spread the virus over a long distance. Additionally, the lack of poultry farms within 10 km of the area where the buzzard carcass was found may partially explain why no outbreak occurred.

Since clade 2.3.2 was first isolated from a dead Chinese pond heron in Hong Kong in 2004, it has spread geographically and evolved genetically. A new fourth-order clade, 2.3.2.1, was recently identified, and A/common buzzard/Bulgaria/38WB/2010 was classified in this clade (8). The question that arises now that clade 2.3.2.1 has spread from Asia to Europe is whether it can cause a scenario similar to that caused by clade 2.2 from 2005–2006, when HPAIV (H5N1) killed millions of birds in Asia, Europe, and Africa. Although no new HPAIV (H5N1)–related events have been reported in Europe since March 2010, some of the aspects of the 2.3.2.1 clade make it difficult to predict the consequences of the clade’s arrival on the continent. For example, this clade is already widely distributed in Asia and is being perpetuated in many wild bird species, which is a prerequisite for long-distance distribution through migration. Wild bird species infected with HPAIV (H5N1) from clade 2.3.2.1 include gray herons, peregrine falcons, and great egrets in Hong Kong; whooper swans, ruby shelducks, and bar-headed geese in Mongolia; and grebes and black-headed gulls in Tyva (8).

The potential of clade 2.3.2.1 HPAIV (H5N1) to cause an outbreak is heightened because vaccines currently in use do not efficiently protect poultry flocks from a strain of this clade that was recently identified in Vietnam (40). Now that clade 2.3.2.1 has spread to Europe, implementing active surveillance plans in all high-risk areas and monitoring the wild birds in the region will play key roles in early detection of incidences of HPAIV (H5N1) infection and in prevention of outbreaks. The expansion of the geographic distribution of HPAIV (H5N1) in wild birds and poultry and the virus’s repeated interspecies transmission to humans make this virus a substantial pandemic threat.
Clade 2.3.2 is widely distributed in Asia, particularly in China, Hong Kong, Korea, Vietnam, Laos, Bangladesh, Nepal, Mongolia, and the Tyva Republic; it is also distributed in eastern Europe, mainly in Romania and Bulgaria (8,9). Tyva is part of the Siberian Federal District of Russia, which is located north of Mongolia.
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